Earliest giant panda false thumb suggests conflicting demands for locomotion and feeding

Of the many peculiarities that enable the giant panda (Ailuropoda melanoleuca), a member of the order Carnivora, to adapt to life as a dedicated bamboo feeder, its extra “thumb” is arguably the most celebrated yet enigmatic. In addition to the normal five digits in the hands of most mammals, the giant panda has a greatly enlarged wrist bone, the radial sesamoid, that acts as a sixth digit, an opposable “thumb” for manipulating bamboo. We report the earliest enlarged radial sesamoid, already a functional opposable “thumb,” in the ancestral panda Ailurarctos from the late Miocene site of Shuitangba in Yunnan Province, China. However, since the late Miocene, the “thumb” has not enlarged further because it must be balanced with the constraints of weight bearing while walking in a plantigrade posture. This morphological adaptation in panda evolution thus reflects a dual function of the radial sesamoid for both bamboo manipulation and weight distribution. The latter constraint could be the main reason why the panda’s false thumb never evolved into a full digit. This crude “thumb” suggests that the origin of the panda’s dedicated bamboo diet goes back to as early as 6–7 Ma.

and historical range (yellow) [16][17][18] , present approximate bamboo forest distribution in China (green) 19 , and Pleistocene and later fossil distribution (solid and open black circles and triangles) 16,[18][19][20][21][22][23][24] . We eliminated the humerus record from Zhoukoudian locality 1 following Jiangzuo et al. 25 2D-F) and one of A. yuanmouensis (Fig. 2G) are available and offer a sense of the variation within and between species. The three M2s from Lufeng display a range of morphology: presence or absence of a lingual cingulum and reduction of buccal cingulum, and presence or absence of a clearly delineated metaconule (RMe3 in Jiangzuo et al. 27 ). Of these, the Shuitangba M2 (ZT-2015-0124) has a distinct lingual cingulum but lacks an elevated metaconule. The Lufeng sample, however, consistently has a more distinct ridge on the lingual side of the preparacrista (RPa1.2 in Jiangzuo et al. 27 ) not seen in ZT-2015-0124. An M2 of A. yuanmouensis has substantially less crenulation in its trigon, whereas its talon has achieved the level of complexity seen in those from Lufeng and Shuitangba. The overall proportion of the Shuitangba M2 is slightly more elongated than in the Lufeng sample and the elevated talon anterocentrally is not seen in the Lufeng M2s. Since M2s in Ailuropoda are more quadrate with greater width to length ratios (Table 1), the narrower ZT-2015-0124 appears slightly more primitive. Given the above dental comparisons, the Shuitangba M2 reliably belongs to Ailurarctos, in terms of both the length/width proportions and the detailed cusp morphology, and we tentatively assign it to Ailurarctos cf. A. lufengensis pending additional materials becoming available.
Among carnivorans, ursids have the most complex molars due to their unique morphology related to hypocarnivory. Within ursids, dental patterns in ailuropodines are some of the most elaborate, with numerous, highly distinct crown cuspules 27 , advantageous for crushing tough bamboo, i.e., durophagous mastication 20 . These features are associated with a robust mandible 28 and lateral movements of the temporomandibular joint 29 . It is evident that the dental pattern of Ailurarctos has reached the level of complexity of modern Ailuropoda, as recognized by Qiu and Qi 14 . In fact, the degree of enamel crenulation on most M2s of Ailurarctos is even greater than in Ailuropoda. If it is accepted that the robust cuspation in Ailuropoda is linked to a bamboo diet, dental specializations in Ailurarctos strongly suggest both an ancestral relationship to Ailuropoda as well as a diet including bamboo 20   , resembles in all essential details those of Ailuropoda previously described 10,12,30 . Compared to those of Indarctos arctoides, a possible stem ailuropodine in the late Miocene of Spain, the Ailurarctos radial sesamoid is considerably larger, relatively wider, and more hooked (see relative size of radial sesamoid to metacarpal I of I. arctoides in Fig. 8 of Abella et al. 9 ), although we lack knowledge of Ailurarctos metacarpals and Abella et al. did not publish lengths of metacarpal I. The proximal articulating facets are also much larger with a more concave facet for the scapholunar in Ailurarctos, while the distal end of the I. arctoides radial sesamoid still preserves a possible cartilaginous tip (see Fig. 3 of Abella et al. 9 ), which is also present in some extant Ailurus 7 but presumably absent in Ailurarctos (lacking a distinct rim seen in Indarctos). The radial sesamoid of Ailurarctos is slightly larger than those of modern pandas, by 8% if compared to the maximum length of the largest radial sesamoid of living panda measured by Li and others 31 , but relative to body size (using M2 length as a proxy), it is significantly larger than its modern counterparts ( Table 2). It is gently convex on the external (approximately ventral) surface and concave on the internal surface (orientation assuming a plantigrade posture). At the proximal end, a large, elongate, concave facet (16 mm in maximum longitudinal dimension) articulates with the medial process of the scapholunar, whereas a much smaller, oval-shaped, flat facet (7 × 9 mm) articulates with the medial face of the first metacarpal. The distal end thickens slightly and bends toward the palm, as if to oppose to the fingers.
Besides its comparatively large size, the radial sesamoid in Ailurarctos differs from that in modern Ailuropoda in other ways. A prominent tubercle arising from the inner edge of the articular facet for the scapholunar, presumably for the attachment of the opponens pollicis muscle 10,32 , is present in ZT-2015-0056 but is not seen in living Ailuropoda. Of more importance, a distinct hook in the distal end 10,32 , bending sharply inward toward the palm (Fig. 4C), and a correspondingly flattened external surface due to the thinning of the distal plate (Fig. 5C, D), both evident in extant Ailuropoda, are not present in Ailurarctos (see Dual Functions below for their functional significance). This flattened external, distal end corresponds to the accessory pad for the false thumb of the panda (Fig. 5E).

Dual functions of false thumb.
Best developed in humans and their close relatives, precision grip by a true opposable thumb (capable of closure of the pollex to opposing fingers) requires not only flexibility of the joints but also complex interactions of flexor and extensor muscles. Endo et al. 33 demonstrated that grasping in pandas is fundamentally different from that in humans. Instead of a human thumb that is capable of independent movements against other fingers, the panda's radial sesamoid forms a functional complex in rigid articulation with the first metacarpal and scapholunar, which collectively rotate with other metacarpals. Once www.nature.com/scientificreports/ fully flexed, the radial sesamoid functional complex couples with the pisiform on the lateral side of the hand to function as a double stop against the pincer-like actions of the bending phalanges (but see Fig. 6, which shows only the radial sesamoid is used in the pincer action and the pisiform is not). Small muscles (such as abductor pollicis brevis and opponens pollicis) between the radial sesamoid and first metacarpal serve as a cushion for the bamboo stems grasped between the radial sesamoid and phalanges (Fig. 5). Such a passive system of gripping, far less effective than that of humans, nonetheless offers the panda the tightness of grip it needs for bamboo feeding. Furthermore, from an evolutionary point of view, such a simple passive mechanism of grasping can be www.nature.com/scientificreports/ functionally useful even with a slight initial enlargement of the radial sesamoid. Natural selection would be effective from the early stages of enlargement, i.e., even a small, protruding lump at the wrist can be a modest help in preventing bamboo from slipping off bent fingers. Radial sesamoids in living giant pandas have a rather abrupt, inward hook near the distal end (Figs. 4C, 5B, 7) as illustrated by Wood-Jones 30 and Endo et al. 32 , and described by Davis 10 and Wang et al. 12 . The function of this hook can be intuitively understood as a passive pincer in a single element grasping system, in contrast to that in humans with a two-segmented pollex in which the distal segment can be bent to facilitate grasping (Fig. 5). The lack of a distal hook in Ailurarctos indicates a two-step evolution, with an initial simple elongation in the false thumb followed by the subsequent appearance of a more refined distal hook (perhaps by late Pleistocene 12 ), concomitant with a slight shortening of the tip.
The radial sesamoid in Ailurarctos exceeds that of its modern descendants, both in absolute and relative size (radial sesamoid index = 1.89 for Ailurarctos from Shuitangba; 0.92 for Shuanghe Cave fossil; 0.84-1.28 for living Ailuropoda melanoleuca) ( Tables 1, 2). If a longer radial sesamoid alone was being selected, it would be expected that modern pandas would have increased the length of the radial sesamoid in the intervening six million years. Yet, modern pandas have a shorter radial sesamoid relative to their increased body size (as compared to their fossil ancestors), adding only a slight hook at the distal end. This raises the question of why the false thumb of pandas did not elongate further, as a longer digit would surely enhance capabilities for grasping thicker bundles of bamboo.
We propose that the lack of further elongation is the result of a functional compromise between the need for grasping larger bundles of bamboo and the weight-bearing function of the false thumb (Fig. 5). All ursids are fully plantigrade in their standing postures, i.e., the palm of the hand touches the ground while walking. A highly elongate radial sesamoid designed for bamboo manipulation would inevitably result in a conflict with walking long distances, thus compromising the radial sesamoid's dual functions-its inner surface for grasping (Fig. 5B) and its outer surface for weight bearing (Fig. 5D). Due to its position in plantigrade posture, any further enlargement of the radial sesamoid would result in greater ventral protrusion and interference with walking. We view the flattened distal surface of the Ailuropoda radial sesamoid as a means to spread the load within the external accessory pad to cushion stride impact, an additional feature indicative of the dual functional demands of the radial sesamoid in both food procurement and locomotion. Living giant pandas thus balance these conflicting demands with a sharp bend inward on the distal end to form a hook and, at the same time, reducing external protrusion by flattening the external walking surface of the false thumb (Fig. 7).
As illustrated in the evolution of the false thumb (Fig. 5), more efficient consumption of bamboo cannot override requirements for weight-bearing while walking because the panda inherited a plantigrade posture. Potential alternatives to overcome such a constraint include a digitigrade posture (lifting the palm off the ground, freeing the wrist area from weight bearing), as in cursorial carnivorans (canids, felids, hyaenids), but this may not have been feasible for ursids given their evolutionary history of plantigrady in addition to arboreality. All digitigrade families evolved from a small, agile ancestor and efficient digitigrady evolved over millions of years, in contrast to ursids who were already large-bodied by the late Miocene and fully plantigrade 36 . Furthermore, pandas are Table 1. Comparison of dental measurements (in mm).

Ailurarctos yuanmouensis
Zong 15 Qiu and Qi 14 ZT-2015-0124 Jin et al. 20 Jin et al. 20 Pei 49 Colbert and Hooijer 50   30 . Note the small distal hook and flat ventral surface of the radial sesamoid in extant Ailuropoda, which are derived features that function for better grasping (small hook) as well as walking (flattened palm surface) in contrast to the primitive conditions seen in Ailurarctos (Fig. 3).  (Fig. 6) to cushion the radial sesamoid 10 , signaling the importance of the weight-bearing function for this bone. While the panda solution may not be the most elegant, its functionality is evidenced by a long history of at least 6-7 million years (Fig. 1).

Grasp volume and grip strength.
The abundance of bamboo in the giant panda's habitat makes daily foraging distance a very small component of the feeding strategy. Instead, eating fast and in large quantities appear to be of greater importance 37 . Perhaps the most demanding function of the false thumb is to maintain a tight grip on bamboo stems while the panda uses its teeth to tear and shred stems into bite size portions for consumption. The high strength of bamboo, especially the woody stems during the winter months, requires considerable grip strength by the hands to twist and jerk, countering the powerful biting and tearing by the jaws (see, for example, a panda cam at the San Diego Zoo: https:// www. faceb ook. com/ watch/ live/?v= 56235 13541 70625 & ref= watch_ perma link). Therefore, it seems likely that a tight grip is more critical to panda's feeding ability than the volume of their grasp.

Radial sesamoid
Fleshy pad for pisiform Fleshy pad for radial sesamoid  20 . The largest species, Ailuropoda baconi, was thought to be restricted to middle and late Pleistocene, with the modern species, A. melanoleuca, as Holocene 20 , although Sheng et al. 34 recognized the initial divergence of the living lineage in the late Pleistocene. The false thumb from late Pleistocene Shuanghe Cave was adopted from Wang et al. 10  www.nature.com/scientificreports/ The strength of the giant panda grip is dependent on the flexor muscles of the fingers, with the radial sesamoid acting as a passive stop against flexion of the fingers. Pandas are good climbers, especially for evading danger 37 , which necessitates powerful digital flexor muscles for the claws to penetrate into tree bark. Such musculature also serves well for gripping bamboo during feeding. Because of the functional constraints imposed on the length of the radial sesamoid noted above, pandas never evolved sufficiently long false thumbs to seize large bundles of bamboo, a task that, while desirable, is not critical for survival. It is instead the ability to grip tightly on bamboo stems to oppose strong twisting forces by the jaws that is essential and on which selection has acted. While the giant panda's false thumb is not the most elegant or dexterous, the persistence of this distinctive morphology for the last six million years suggests that it has fulfilled an essential function for survival of the lineage.
Bulk feeding as a tradeoff in low quality but year-round availability of bamboo. Besides having a false thumb, much else about the giant panda is also unusual and/or enigmatic. Pandas traded the high-protein, omnivorous diet of their ursid ancestors for bamboo, a woody grass of high fiber and low nutrition, but with year-round availability in South China and Southeast Asia. To make this tradeoff work, pandas eat prodigious quantities of bamboo, up to 45 kg/day (depending on the season), and spend ~ 15 h/day eating 37 . The panda's short digestive tract, inherited from its carnivoran ancestors, is also poorly suited for extracting nutrients, absorbing less than 20% of digestible dry matter 38 . Furthermore, pandas lack the high-crowned teeth that most ungulate mammals possess for grinding tough plant fibers into a fine mush and consequently make minimal use of microbials to break down cellulose to extract the structural carbohydrates 11 . As a result, the panda's gastrointestinal tract allows a rapid passage of digesta in less than 12 h 38 , too fast for fermentation when compared to fore-and hindgut fermenting mammalian herbivores, and necessitating an equally prodigious quantity of defecation, up to 100 times/day 39 .
This extreme bulk feeding strategy thus prioritizes dietary quantity over nutritional quality and nutrient extraction rate. This is made possible by the wide availability of bamboo, practically eliminating energy expenditure for foraging while maximizing the net rate of energy intake 40 . In modern panda habitats, bamboo (such as Fargesia and Sinarundinaria) are in plentiful, year-round supply, typically more than what pandas can consume (except during periodical bamboo flowering and die outs). With 99% of their food being bamboo and without major competitors for this abundant food resource, nor the need to avoid predators, pandas can thus reduce daily foraging range to within tens of meters of their resting dens, permitting a highly efficient foraging strategy of spending large portions of daily activities feeding and resting within small areas 37 .
Pandas usually feed while sitting, hooking bamboo stems toward the mouth using curved paws and while biting the leaves/stems, use grasping hands to jerk the stems up and down to help sever them 37 . The hands are also capable of a twisting action to tear off strips in the mouth, which requires a tight grip. It is difficult to imagine www.nature.com/scientificreports/ that the panda's crude false thumb can be useful for conventional omnivorous purposes such as gathering of seeds, nuts, berries, or even low grasses, suggesting that the sole dietary purpose of an enlarged radial sesamoid is bamboo feeding, although a tree-climbing function for the false thumb has been suggested for ailurids 6,7 . If the dietary function is paramount, the panda's false thumb must be a crucial adaptation for efficient bamboo procurement within this lineage. Once pandas committed to this bulk feeding strategy, the false thumb was an advantageous solution to the challenge of bamboo manipulation. Despite the seeming inefficiency of its digestive system, the giant panda's bulk feeding strategy permitted it to successfully expand to much of South China and Southeast Asia and become a prominent member of the Giant Panda-Stegodon fauna in the Pleistocene 41 (Fig. 1). Deep inside the Chinese bamboo forests, giant pandas adopt a solitary, reclusive life of quiet herbivory, retreating from the more dominant position in the food chain of their distant relatives. In adopting a low-quality, year-round bamboo diet, pandas are also unable to store sufficient fat to hibernate, a crucial strategy for ursids to expand into high latitudes and to migrate across Beringia into North America 42,43 . The panda's historic range is thus consistent with both the availability of bamboo and a warm climate without the need for hibernation ( Fig. 1; note that a previous purported panda record from Zhoukoudian locality 1 44 , a jarring presence in a cold climate, has now been shown to be that of a cave bear 25 ).
The panda's transition from a broad, omnivorous diet to a highly specialized bamboo diet necessitated multiple changes in anatomy and physiology, as well as their genetics underpinning [45][46][47] . However, even after at least six million years of a bamboo diet, these transformations are still limited, mostly focused on food handling while the digestive system remains that of a carnivore 48 . The fact that there was no further elongation of the false thumb in the panda lineage after the late Miocene, suggests that an adequate grip for bamboo had been obtained, i.e., good enough for grasping a single stem or small bundle, and that further enlargement was inhibited by countervailing selection for weight-bearing and walking (Fig. 8). We caution, however, that the fossil record is too incomplete to allow a full understanding of this process and future discoveries will likely reveal unforeseen details.
Steven J. Gould's 4 insightful remarks still stand: "the panda's true thumb is committed to another role, too specialized for a different function to become an opposable, manipulating digit. So the panda must use parts on hand and settle for an enlarged wrist bone and a somewhat clumsy, but quite workable, solution". However, he would probably have been delighted to learn that the historic contingency of the panda's false thumb requires that while being a better finger was favored by selection, it also had to bear the burden of considerable body weight.

Data availability
All data generated or analysed during this study are included in this published article and its supplementary information files.